Coral Holobiont Research Articles

Microbiomes of Healthy and Bleached Corals During a 2016 Thermal Bleaching Event in the Andaman Sea of Thailand

As seawater temperature rises, repeated thermal bleaching events have negatively affected the reefs of the Andaman Sea for over decades. Studies on the coral-associated microbial diversity of prokaryotes and microbial eukaryotes (microbiome) in healthy and bleached corals are important to better understand the coral holobionts that involved augmented resistance to stresses, and this information remains limited in the Andaman Sea of Thailand. The present study thereby described the microbiomes of healthy (unbleached) and bleached colonies of four prevalent corals, Acropora humilis, Platygyra sp., Pocillopora damicornis, and Porites lutea, along with the surrounding seawater and sediments, that were collected during a 2016 thermal bleaching event, using 16S and 18S rRNA genes next-generation sequencing (NGS). Both prokaryotic and eukaryotic microbes showed isolated community profiles among sample types (corals, sediment, and seawater) [analysis of similarities (ANOSIM): p = 0.038 for prokaryotes, p < 0.001 for microbial eukaryotes] and among coral genera (ANOSIM: p < 0.001 for prokaryotes and microbial eukaryotes). In bleached state corals, we found differences in microbial compositions from the healthy state corals. Prevalent differences shared among bleached coral genera (shared in at least three coral genera) included a loss of reported coral-beneficial microbes, such as Pseudomonadales, Alteromonadales, and Symbiodinium; meanwhile an increase of putative coral-pathogenic Malassezia and Aspergillus. This difference could affect carbon and nitrogen availability for coral growth, reflective of a healthy or bleached state. Our findings in part supported previously microbial dysbiosis knowledge of thermal bleaching coral microbiomes around South East Asia marine geography, and together ongoing efforts are to support the understanding and management of microbial diversity to reduce the negative impacts to corals in massive thermal bleaching events.

High-Resolution Dynamics of Hydrogen Peroxide on the Surface of Scleractinian Corals in Relation to Photosynthesis and Feeding

We developed and used a microsensor to measure fast (<1 s) dynamics of hydrogen peroxide (H2O2) on the polyp tissue of two scleractinian coral species (Stylophora pistillata and Pocillopora damicornis) under manipulations of illumination, photosynthesis, and feeding activity. Our real-time tracking of H2O2 concentrations on the coral tissue revealed rapid changes with peaks of up to 60 μM. We observed bursts of H2O2 release, lasting seconds to minutes, with rapid increase and decrease of surficial H2O2 levels at rates up to 15 μM s–1. We found that the H2O2 levels on the polyp surface are enhanced by oxygenic photosynthesis and feeding, whereas H2O2 bursts occurred randomly, independently from photosynthesis. Feeding resulted in a threefold increase of baseline H2O2 levels and was accompanied by H2O2 bursts, suggesting that the coral host is the source of the bursts. Our study reveals that H2O2 levels at the surface of coral polyps are much higher and more dynamic than previously reported, and that bursts are a regular feature of the H2O2 dynamics in the coral holobiont.

Significant Changes in Bacterial Communities Associated with Pocillopora Corals Ingestion by Crown-of-Thorns Starfish: An Important Factor Affecting the Coral's Health.

Coral ingestion by crown-of-thorns starfish (COTS) is an important cause of coral reef degradation, although the impacts of COTS feeding on coral-associated microbial communities are not well understood. Therefore, in this study, we analyzed the coral tissue-weight, Symbiodiniaceae density (SD), bacterial community composition, and the predicted functions of bacterial genes associated with Pocillopora corals in healthy portions and feeding scars, following COTS feeding. Coral tissue-weight loss rate in the feeding scars was 71.3–94.95%. The SDs were significantly lower in the feeding scars, and the SD-loss rate was 92.05% ± 2.12%. The relative abundances of bacterial communities associated with Pocillopora corals after COTS feeding changed significantly and were almost completely reorganized at the phylum and genus levels. Analysis of the microbial metagenomic-functional capacities showed that numerous physiological functions of the coral-bacterial holobionts in the feeding scars were different, including amino acid metabolism, xenobiotic biodegradation and metabolism, lipid metabolism, membrane transport, signal transduction, and cell motility, and all these capacities could be corroborated based on metagenomic, transcriptomic or proteomic technologies. Overall, our research suggests that coral holobionts may be destroyed by COTS, and our findings imply that bacterial communities in feeding scars could affect the health of Pocillopora corals.

Diversity and Distribution of Microbial Communities Associated with Reef Corals of the Malay Peninsula.

Coral-associated bacteria play critical roles in the regulation of coral health and function. Environmental perturbations that alter the bacterial community structure can render the coral holobiont more susceptible and less resilient to disease. Understanding the natural variation of the coral microbiome across space and host species provides a baseline that can be used to distinguish shifts in community structure. Using a 16S rRNA gene metabarcoding approach, this study examines bacterial community structure across three scleractinian coral hosts. Our results show that corals of three regions-eastern and western Peninsular Malaysia and Singapore-host distinct bacterial communities; despite these differences, we were able to identify a core microbiome shared across all three species. This core microbiome was also present in samples previously collected in Thailand, suggesting that these core microbes play an important role in promoting and maintaining host health. For example, several have been identified as dimethylsulfoniopropionate (DMSP) metabolizers that have roles in sulfur cycling and the suppression of bacterial pathogens. Pachyseris speciosa has the most variable microbiome, followed by Porites lutea, with the composition of the Diploastrea heliopora microbiome the least variable throughout all locations. Microbial taxa associated with each region or site are likely shaped by local environmental conditions. Taken together, host identity is a major driver of differences in microbial community structure, while environmental heterogeneity shapes communities at finer scales.

Antibiotics Alter Pocillopora Coral-Symbiodiniaceae-Bacteria Interactions and Cause Microbial Dysbiosis During Heat Stress

Symbioses between eukaryotes and their associated microbial communities are fundamental processes that affect organisms’ ecology and evolution. A unique example of this is reef-building corals that maintain symbiotic associations with dinoflagellate algae (Symbiodiniaceae) and bacteria that affect coral health through various mechanisms. However, little is understood about how coral-associated bacteria communities affect holobiont heat tolerance. In this study, we investigated these interactions in four Pocillopora coral colonies belonging to three cryptic species by subjecting fragments to treatments with antibiotics intended to suppress the normal bacteria community, followed by acute heat stress. Separate treatments with only antibiotics or heat stress were conducted to compare the effects of individual stressors on holobiont transcriptome responses and microbiome shifts. Across all Pocillopora species examined, combined antibiotics and heat stress treatment significantly altered coral-associated bacteria communities and caused major changes in both coral and Cladocopium algal symbiont gene expression. Individually, heat stress impaired Pocillopora protein translation and activated DNA repair processes, while antibiotics treatments caused downregulation of Pocillopora amino acid and inorganic ion transport and metabolism genes and Cladocopium photosynthesis genes. Combined antibiotics-heat stress treatments caused synergistic effects on Pocillopora and Cladocopium gene expression including enhanced expression of oxidative stress response genes, programed cell death pathways and proteolytic enzymes that indicate an exacerbated response to heat stress following bacteria community suppression. Collectively, these results provide further evidence that corals and their Symbiodiniaceae and bacteria communities engage in highly coordinated metabolic interactions that are crucial for coral holobiont health, homeostasis, and heat tolerance.

Short communication: Algal genotypes in White Syndrome infected coral Acropora muricata from the Karimunjawa Islands, Indonesia

Abstract. Wijayanti DP, Nadia M, Indrayanti E, Haryanti D, Bachtiar M. 2021. Short communication: Algal genotypes in White Syndrome infected coral Acropora muricata from the Karimunjawa Islands, Indonesia. Biodiversitas 23: 415-423. The physiological equilibrium of the coral holobiont may help the corals to survive under various environmental threats. The symbiont genotype is thought to play an important role in the host's susceptibility to thermal stress and coral disease incidence. We identified the Symbiodiniaceae diversity of coral Acropora muricata infected by White Syndrome (WS). Samples were collected from Cemara Kecil Island and Barakuda Beach, Kemujan Island, Karimunjawa Islands. We applied DNA barcoding of 28S nuclear ribosomal RNA gene of the healthy colonies, healthy tissue, and lesions of diseased colonies to perform their symbiont type identification. There were two different symbiont types observed from the phylogenetic analysis, which formed two clades. A clade consisting all Cemara Kecil Island samples while the other with all Barakuda Beach samples except for one. All samples harbored symbiont types from the genus Cladocopium. The members of the genus were reported to have various physiological properties which may support the host resilience when facing the disease. A robust study is needed to reveal the influence of symbiont genotypes on the occurrence of coral disease and the susceptibility of the coral host.

Lagoon coral microbiomes and their potential relationship with adaptation of coral holobionts to extreme high-temperature environments

Numerous corals can survive in high-temperature environments, but little attention has been paid to the microbiome of lagoon corals and their potential adaptation to thermal environments. In this study, we explored this issue by analyzing the coral-symbiotic Symbiodiniaceae, Symbiodiniaceae densities, and bacterial communities among coral species and seawater in the lagoon regions of the southern South China Sea (SCS). Galaxea fascicularis had the highest Symbiodiniaceae density and relative abundance of heat-tolerant Symbiodiniaceae (Durusdinium trenchii), and Acropora cytherea had the lowest density, but the highest diversity, of Symbiodiniaceae. The Symbiodiniaceae diversity of Fungia fungites was the lowest. Moreover, the Symbiodiniaceae community and diversity differed significantly between the lagoon and open-ocean seawater. In addition, the relative abundance of Vibrio was higher in coral holobionts than in the lagoon seawater samples. The relative abundance of Ruegeria was highest in A. cytherea, indicating that coral-associated bacteria in the lagoon were affected by high thermal stress during summer. However, corals in the lagoon may adopt different adaptation strategies for high-temperature environments. G. fascicularis corals may adapt to lagoon environments by symbiosis with heat-tolerant Symbiodiniaceae at high densities and abundance, whereas A. cytherea may survive in the lagoon environment based on a highly flexible symbiosis associated with the high photosynthetic efficiency of Symbiodiniaceae and bacteria.

Multi-Omics Revealing the Response Patterns of Symbiotic Microorganisms and Host Metabolism in Scleractinian Coral Pavona minuta to Temperature Stresses.

Global climate change has resulted in large-scale coral reef decline worldwide, for which the ocean warming has paid more attention. Coral is a typical mutually beneficial symbiotic organism with diverse symbiotic microorganisms, which maintain the stability of physiological functions. This study compared the responses of symbiotic microorganisms and host metabolism in a common coral species, Pavona minuta, under indoor simulated thermal and cold temperatures. The results showed that abnormal temperature stresses had unfavorable impact on the phenotypes of corals, resulting in bleaching and color change. The compositions of symbiotic bacteria and dinoflagellate communities only presented tiny changes under temperature stresses. However, some rare symbiotic members have been showed to be significantly influenced by water temperatures. Finally, by using ultra-performance liquid chromatography tandem mass spectrometry (UPLC–MS) method, we found that different temperature stresses had very different impacts on the metabolism of coral holobiont. The thermal and cold stresses induced the decrease of anti-oxidation metabolites, several monogalactosyldiacylglycerols (MGDGs), and the increase of lipotoxic metabolite, 10-oxo-nonadecanoic acid, in the coral holobiont, respectively. Our study indicated the response patterns of symbiotic microorganisms and host metabolism in coral to the thermal and cold stresses, providing theoretical data for the adaptation and evolution of coral to a different climate in the future.

Regulation of the Coral-Associated Bacteria and Symbiodiniaceae in Acropora valida Under Ocean Acidification.

Ocean acidification is one of many stressors that coral reef ecosystems are currently contending with. Thus, understanding the response of key symbiotic microbes to ocean acidification is of great significance for understanding the adaptation mechanism and development trend of coral holobionts. Here, high-throughput sequencing technology was employed to investigate the coral-associated bacteria and Symbiodiniaceae of the ecologically important coral Acropora valida exposed to different pH gradients. After 30 days of acclimatization, we set four acidification gradients (pH 8.2, 7.8, 7.4, and 7.2, respectively), and each pH condition was applied for 10 days, with the whole experiment lasting for 70 days. Although the Symbiodiniaceae density decreased significantly, the coral did not appear to be bleached, and the real-time photosynthetic rate did not change significantly, indicating that A. valida has strong tolerance to acidification. Moreover, the Symbiodiniaceae community composition was hardly affected by ocean acidification, with the C1 subclade (Cladocopium goreaui) being dominant among the Symbiodiniaceae dominant types. The relative abundance of the Symbiodiniaceae background types was significantly higher at pH 7.2, indicating that ocean acidification might increase the stability of the community composition by regulating the Symbiodiniaceae rare biosphere. Furthermore, the stable symbiosis between the C1 subclade and coral host may contribute to the stability of the real-time photosynthetic efficiency. Finally, concerning the coral-associated bacteria, the stable symbiosis between Endozoicomonas and coral host is likely to help them adapt to ocean acidification. The significant increase in the relative abundance of Cyanobacteria at pH 7.2 may also compensate for the photosynthesis efficiency of a coral holobiont. In summary, this study suggests that the combined response of key symbiotic microbes helps the whole coral host resist the threats of ocean acidification.

Proteome and microbiota analyses characterizing dynamic coral-algae-microbe tripartite interactions under simulated rapid ocean acidification

Ocean acidification (OA) is a pressing issue currently and in the future for coral reefs. The importance of maintenance interactions among partners of the holobiont association in the stress response is well appreciated; however, the candidate molecular and microbial mechanisms that underlie holobiont stress resilience or susceptibility remain unclear. Here, to assess the effects of rapid pH change on coral holobionts at both the protein and microbe levels, combined proteomics and microbiota analyses of the scleractinian coral Galaxea fascicularis exposed to three relevant OA scenarios, including current (pHT = 8.15), preindustrial (pHT = 8.45) and future IPCC-2100 scenarios (pHT = 7.85), were conducted. The results demonstrated that pH changes had no significant effect on the physiological calcification rate of G. fascicularis in a 10-day experiment; however, significant differences were recorded in the proteome and 16S profiling. Proteome variance analysis identified some of the core biological pathways in coral holobionts, including coral host infection and immune defence, and maintaining metabolic compatibility involved in energy homeostasis, nutrient cycling, antibiotic activity and carbon budgets of coral-Symbiodiniaceae interactions were key mechanisms in the early OA stress response. Furthermore, microbiota changes indicate substantial microbial community and functional disturbances in response to OA stress, potentially compromising holobiont health and fitness. Our results may help to elucidate many complex mechanisms to describe scleractinian coral holobiont responses to OA and raise interesting questions for future studies.

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.

Gene clusters for biosynthesis of mycosporine-like amino acids in dinoflagellate nuclear genomes: Possible recent horizontal gene transfer between species of Symbiodiniaceae (Dinophyceae).

Global warming increases the temperature of the ocean surface, which can disrupt dinoflagellate‐coral symbioses and result in coral bleaching. Photosynthetic dinoflagellates of the family Symbiodiniaceae include bleaching‐tolerant and bleaching‐sensitive coral symbionts. Therefore, understanding the molecular mechanisms for changing symbiont diversity is potentially useful to assist recovery of coral holobionts (corals and their associated microbes, including multiple species of Symbiodiniaceae), although sexual reproduction has not been observed in the Symbiodiniaceae. Recent molecular phylogenetic analyses estimate that the Symbiodiniaceae appeared 160 million years ago and diversified into 15 groups, five genera of which now have available draft genomes (i.e., Symbiodinium, Durusdinium, Breviolum, Fugacium, and Cladocopium). Comparative genomic analyses have suggested that crown groups have fewer gene families than early‐diverging groups, although many genes that were probably acquired via gene duplications and horizontal gene transfers (HGTs) have been found in each decoded genome. Because UV stress is likely a contributor to coral bleaching, and because the highly conserved gene cluster for mycosporine‐like amino acid (MAA) biosynthesis has been found in thermal‐tolerant symbiont genomes, I reviewed genomic features of the Symbiodiniaceae, focusing on possible acquisition of a biosynthetic gene cluster for MAAs, which absorb UV radiation. On the basis of highly conserved noncoding sequences, I hypothesized that HGTs have occurred among members of the Symbiodiniaceae and have contributed to the diversification of Symbiodiniaceae–host relationships. Finally, I proposed that bleaching tolerance may be strengthened by multiple MAAs from both symbiotic dinoflagellates and corals.

Ectohydrolytic enzyme activities of bacteria associated with Orbicella annularis coral

Ectohydrolytic enzyme activity (EEA) potential of 37 bacterial isolates derived from Orbicella annularis coral and 2 coral pathogens (Vibrio shilonii and V. coralliilyticus) was measured as model to infer the role of bacteria in organic matter processing within coral reef ecosystems. Bacterial cell-specific activities of eight enzyme types were measured after incubation in organic matter enriched and unenriched filtered seawater. Max value of activities of alkaline phosphatase, oleate-lipase, stearate-lipase and proteinase were 769.3, 327.6, 82.9 and 36.7 amol cell−1 h−1, respectively. Chitinase, α-mannosidase, α-glucosidase and β-glucosidase were generally lower by comparison (max 4.7–20.7 amol cell−1 h−1). No “super” isolates (bacteria expressing high levels of all ectohydrolases) were found suggesting a “specialization” among individual bacterial strains. Cumulatively, the 39 isolates tested displayed a broad range of cell-specific enzyme activities in both organic matter conditions. Culture-independent measurement of coral mucus layer EEA in O. annularis off a Panama reef showed comparable EEA patterns and diversity as the isolates. Volume-specific EEAs of all enzymes except alkaline phosphatase were 8–48 times higher in mucus than in surrounding seawater (SSW) samples. However, cell-specific EEAs in mucus were generally lower than in the SSW partly due to more abundant cells in the mucus than in SSW. For field samples, ≥ 85% of proteinase was cell-bound, while lipase was preferentially dissolved (40–96%). In general, the production of dissolved EEAs varied among measurements depending on sample source and enzyme types, suggesting a potential role of ectoenzyme size distribution in linking the whole reef ecosystem. Our findings support that the cumulative ectoenzyme expression (“ectoenzymome”) of the coral microbiome has the potential to maintain the functional resilience of the coral holobiont and response to stress through its contribution to organic matter processing within coral reef ecosystems.

Highly Variable and Non-complex Diazotroph Communities in Corals From Ambient and High CO2 Environments

The ecological success of corals depends on their association with microalgae and a diverse bacterial assemblage. Ocean acidification (OA), among other stressors, threatens to impair host-microbial metabolic interactions that underlie coral holobiont functioning. Volcanic CO2 seeps offer a unique opportunity to study the effects of OA in natural reef settings and provide insight into the long-term adaptations under a low pH environment. Here we compared nitrogen-fixing bacteria (diazotrophs) associated with four coral species (Pocillopora damicornis, Galaxea fascicularis, Acropora secale, and Porites rus) collected from CO2 seeps at Tutum Bay (Papua New Guinea) with those from a nearby ambient CO2 site using nifH amplicon sequencing to characterize the effects of seawater pH on bacterial communities and nitrogen cycling. Diazotroph communities were of generally low diversity across all coral species and for both sampling sites. Out of a total of 25 identified diazotroph taxa, 14 were associated with P. damicornis, of which 9 were shared across coral species. None of the diazotroph taxa, however, were consistently found across all coral species or across all samples within a species pointing to a high degree of diazotroph community variability. Rather, the majority of sampled colonies were dominated by one or two diazotroph taxa of high relative abundance. Pocillopora damicornis and Galaxea fascicularis that were sampled in both environments showed contrasting community assemblages between sites. In P. damicornis, Gammaproteobacteria and Cyanobacteria were prevalent under ambient pCO2, while a single member of the family Rhodobacteraceae was present at high relative abundance at the high pCO2 site. Conversely, in G. fascicularis diazotroph communities were indifferent between both sites. Diazotroph community changes in response to OA seem thus variable within as well as between host species, potentially arguing for haphazard diazotroph community assembly. This warrants further research into the underlying factors structuring diazotroph community assemblages and their functional role in the coral holobiont.

Coastal corals during heat stress and eutrophication: A case study in Northwest Hainan coastal areas

This study initially investigated the coral status during the unexpected bleaching event in three coastal areas in Northwest Hainan coastal areas and analyzed changes in coral holobionts of the healthy and bleached Galaxea fascicularis. Coral coverage had declined severely, and the bleaching rate was extremely high during heat stress. The bleached corals had lower maximum photosynthetic yield, actual photosynthetic yield, zooxanthellae density, and chlorophyll a content than the healthy G. fascicularis, but there was no significant difference in protein, carbohydrate and lipid in eutrophic waters. The diversity and community composition of Symbiodiniaceae and symbiotic bacteria between healthy and bleached G. fascicularis showed no difference. Function prediction of the symbiotic bacteria revealed that the metabolism process was the main pathway of annotation. Present findings suggested that energy reserve functioning and high stability of the holobiont structure and might provide opportunities to G. fascicularis to adapt to eutrophication and heat stress.

Extending the natural adaptive capacity of coral holobionts

Anthropogenic climate change and environmental degradation destroy coral reefs, the ecosystem services they provide, and the livelihoods of close to a billion people who depend on these services. Restoration approaches to increase the resilience of corals are therefore necessary to counter environmental pressures relevant to climate change projections. In this Review, we examine the natural processes that can increase the adaptive capacity of coral holobionts, with the aim of preserving ecosystem functioning under future ocean conditions. Current approaches that centre around restoring reef cover can be integrated with emerging approaches to enhance coral stress resilience and, thereby, allow reefs to regrow under a new set of environmental conditions. Emerging approaches such as standardized acute thermal stress assays, selective sexual propagation, coral probiotics, and environmental hardening could be feasible and scalable in the real world. However, they must follow decision-making criteria that consider the different reef, environmental, and ecological conditions. The implementation of adaptive interventions tailored around nature-based solutions will require standardized frameworks, appropriate ecological risk–benefit assessments, and analytical routines for consistent and effective utilization and global coordination. Anthropogenic climate change and environmental deterioration are driving global degradation of coral reefs. This Review examines how the natural adaptive capacity of coral holobionts can be harnessed and expanded to counter the ongoing loss of coral reefs.

Microbes support enhanced nitrogen requirements of coral holobionts in a high CO2 environment.

Ocean acidification is posing a threat to calcifying organisms due to the increased energy requirements of calcification under high CO2 conditions. The ability of scleractinian corals to cope with future ocean conditions will thus depend on their ability to fulfil their carbon requirement. However, the primary productivity of coral holobionts is limited by low nitrogen (N) availability in coral reef waters. Here, we employed CO2 seeps of Tutum Bay (Papua New Guinea) as a natural laboratory to understand how coral holobionts offset their increased energy requirements under high CO2 conditions. Our results demonstrate for the first time that under high pCO2 conditions, N assimilation pathways of Pocillopora damicornis are jointly modified. We found that diazotroph-derived N assimilation rates in the Symbiodiniaceae were significantly higher in comparison to an ambient CO2 control site, concomitant with a restructured diazotroph community and the specific prevalence of an alpha-proteobacterium. Further, corals at the high CO2 site also had increased feeding rates on picoplankton and in particular exhibited selective feeding on Synechococcus sp., known to be rich in N. Given the high abundance of picoplankton in oligotrophic waters at large, our results suggest that corals exhibiting flexible diazotrophic communities and capable of exploiting N-rich picoplankton sources to offset their increased N requirements may be able to cope better in a high pCO2 world.

Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress

As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures.

Host–symbiont transcriptomic changes during natural bleaching and recovery in the leaf coral Pavona decussata

Coral bleaching has become a major threat to coral reefs worldwide, but for most coral species little is known about their resilience to environmental changes. We aimed to understand the gene expressional regulation underlying natural bleaching and recovery in Pavona decussata, a dominant species of scleractinian coral in the northern South China Sea. Analyzing samples collected in 2017 from the field revealed distinct zooxanthellae density, chlorophyll a concentration and transcriptomic signatures corresponding to changes in health conditions of the coral holobiont. In the host, normal-looking tissues of partially bleached colonies were frontloaded with stress responsive genes, as indicated by upregulation of immune defense, response to endoplasmic reticulum, and oxidative stress genes. Bleaching was characterized by upregulation of apoptosis-related genes which could cause a reduction in algal symbionts, and downregulation of genes involved in stress responses and metabolic processes. The transcription factors stat5b and irf1 played key roles in bleaching by regulating immune and apoptosis pathways. Recovery from bleaching was characterized by enrichment of pathways involved in mitosis, DNA replication, and recombination for tissue repairing, as well as restoration of energy and metabolism. In the symbionts, bleaching corresponded to imbalance in photosystems I and II activities which enhanced oxidative stress and limited energy production and nutrient assimilation. Overall, our study revealed distinct gene expressional profiles and regulation in the different phases of the bleaching and recovery process, and provided new insight into the molecular mechanisms underlying the holobiont's resilience that may determine the species’ fate in response to global and regional environmental changes.

Cross-Linked Regulation of Coral-Associated Dinoflagellates and Bacteria in Pocillopora sp. during High-Temperature Stress and Recovery.

As the problem of ocean warming worsens, the environmental adaptation potential of symbiotic Symbiodiniaceae and bacteria is directly related to the future and fate of corals. This study aimed to analyse the comprehensive community dynamics and physiology of these two groups of organisms in the coral Pocillopora sp. through indoor simulations of heat stress (which involved manually adjusting the temperature between both 26 °C and 34 °C). Heat treatment (≥30 °C) significantly reduced the abundance of Symbiodiniaceae and bacteria by more than 70%. After the temperature was returned to 26 °C for one month, the Symbiodiniaceae density was still low, while the absolute number of bacteria quickly recovered to 55% of that of the control. At this time point, the Fv/Fm value rose to 91% of the pretemperature value. The content of chlorophyll b associated with Cyanobacteria increased by 50% compared with that under the control conditions. Moreover, analysis of the Symbiodiniaceae subclade composition suggested that the relative abundance of C1c.C45, C1, and C1ca increased during heat treatment, indicating that they might constitute heat-resistant subgroups. We suggest that the increase in the absolute number of bacteria during the recovery period could be an important indicator of coral holobiont recovery after heat stress. This study provides insight into the cross-linked regulation of key symbiotic microbes in the coral Pocillopora sp. during high-temperature stress and recovery and provides a scientific basis for exploring the mechanism underlying coral adaptation to global warming.